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Neural mechanism of optimal limb coordination in crustacean swimming.

ABSTRACT: A fundamental challenge in neuroscience is to understand how biologically salient motor behaviors emerge from properties of the underlying neural circuits. Crayfish, krill, prawns, lobsters, and other long-tailed crustaceans swim by rhythmically moving limbs called swimmerets. Over the entire biological range of animal size and paddling frequency, movements of adjacent swimmerets maintain an approximate quarter-period phase difference with the more posterior limbs leading the cycle. We use a computational fluid dynamics model to show that this frequency-invariant stroke pattern is the most effective and mechanically efficient paddling rhythm across the full range of biologically relevant Reynolds numbers in crustacean swimming. We then show that the organization of the neural circuit underlying swimmeret coordination provides a robust mechanism for generating this stroke pattern. Specifically, the wave-like limb coordination emerges robustly from a combination of the half-center structure of the local central pattern generating circuits (CPGs) that drive the movements of each limb, the asymmetric network topology of the connections between local CPGs, and the phase response properties of the local CPGs, which we measure experimentally. Thus, the crustacean swimmeret system serves as a concrete example in which the architecture of a neural circuit leads to optimal behavior in a robust manner. Furthermore, we consider all possible connection topologies between local CPGs and show that the natural connectivity pattern generates the biomechanically optimal stroke pattern most robustly. Given the high metabolic cost of crustacean swimming, our results suggest that natural selection has pushed the swimmeret neural circuit toward a connection topology that produces optimal behavior.

SUBMITTER: Zhang C

PROVIDER: S-EPMC4183325 | biostudies-literature | 2014 Sep

REPOSITORIES: biostudies-literature

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Project description:Lower-limb intersegmental coordination is a complex component of human walking. Aging may result in impairments of motor control and coordination contributing to the decline in mobility inducing loss of autonomy. Investigating intersegmental coordination could therefore provide insights into age-related changes in neuromuscular control of gait. However, it is unknown whether the age-related declines in gait performance relates to intersegmental coordination. The aim of this study was to evaluate the impact of aging on the coordination of lower limb kinematics and kinetics during walking at a conformable speed. We then assessed the body kinematics and kinetics from gait analyses of 84 volunteers from 25 to 85 years old when walking was performed at their self-selected speeds. Principal Component Analysis (PCA) was used to assess lower-limb intersegmental coordination and to evaluate the planar covariation of the Shank-Thigh and Foot-Shank segments. Ankle and knee stiffness were also estimated. Age-related effects on planar covariation parameters was evaluated using multiple linear regressions (i.e., without a priori age group determination) adjusted to normalized self-selected gait velocity. Colinearity between parameters was assessed using a variation inflation factor (VIF) and those with a VIF < 5 were entered in the analysis. Normalized gait velocity significantly decreased with aging (r = -0.24; P = 0.028). Planar covariation of inter-segmental coordination was consistent across age (99.3 ± 0.24% of explained variance of PCA). Significant relationships were found between age and intersegmental foot-shank coordination, range of motion of the ankle, maximal power of the knee, and the ankle. Lower-limb coordination was modified with age, particularly the coordination between foot, and shank. Such modifications may influence the ankle motion and thus, ankle power. This observation may explain the decrease in the ankle plantar flexor strength mainly reported in the literature. We therefore hypothesize that this modification of coordination constitutes a neuromuscular adaptation of gait control accompanying a loss of ankle strength and amplitude by increasing the knee power in order to maintain gait efficiency. We propose that foot-shank coordination might represent a valid outcome measure to estimate the efficacy of rehabilitative strategies and to evaluate their efficiency in restoring lower-limb synergies during walking.

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Neural mechanism of optimal limb coordination in crustacean swimming.

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